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Bernatchez, L.

Publications and source records attributed to Bernatchez, L..

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Domestication and temperature modulate gene expression signatures and growth in the Australasian snapper Chrysophrys auratus

ABSTRACT\n\nIdentifying genes and pathways involved in domestication is critical to understand how species change in response to human-induced selection pressures. We experimentally manipulated temperature conditions for F1-hatchery and wild Australasian snapper (Chrysophrys auratus) for 18 days and measured differences in growth, white muscle RNA transcription and haematological blood parameters. Over 2.2 Gb paired-end reads were assembled de novo for a total set of 33,017 transcripts (N50 = 2,804). We found pronounced growth and gene expression differences between wild and domesticated individuals related to global developmental and immune pathways. Temperature modulated growth responses were linked to major pathways affecting metabolism, cell regulation and signalling. This study is the first step towards gaining an understanding of the changes occurring in the early stages of domestication, and the mechanisms underlying thermal adaptation and associated growth in poikilothermic vertebrates. Our study further provides the first transcriptome resources for studying biological questions in this non-model fish species.

evolutionary biology

Combining population genomics and forward simulations to investigate stocking impacts: A case study of Muskellunge (Esox masquinongy) from the St. Lawrence River basin

Understanding the genetic and evolutionary impacts of fish stocking on wild populations has long been of interest as negative consequences such as reduced fitness and loss of genetic resources are commonly reported. Nearly five decades of extensive stocking of over a million Muskellunge (Esox masquinongy) in the Lower St. Lawrence River (Quebec, Canada) was implemented by managers in an attempt to sustain a fishery. We investigated the effect of stocking on this native species genetic structure and allelic diversity in the St. Lawrence river and its tributaries as well as several stocked inland lakes. Using Genotype-By-Sequencing (GBS), we genotyped 643 individuals representing 22 sampling sites and combined this information with forward simulations to investigate the genetic consequences of stocking. Individuals native to the St. Lawrence watershed were genetically divergent from the sources used for stocking and both the St. Lawrence tributaries and inland lakes were also naturally divergent from the main stem. Empirical data and simulations revealed weak effects of stocking on admixture patterns within the St. Lawrence despite intense stocking in the past, whereas footprints of admixture were higher in the smaller stocked populations from tributaries and lakes. Altogether, our data suggests that selection against introgression has been relatively efficient within the large St. Lawrence River. In contrast, the smaller populations from adjacent tributaries and lakes still displayed stocking related admixture which apparently resulted in higher genetic diversity, suggesting that, while stocking stopped at the same time, its impact remained higher in these populations. Finally, the origin of populations from inland lakes that were established by stocking confirmed their close affinity with these source populations. This study illustrates the benefit of combining extensive genomic data with forward simulations for improved inferences regarding outcomes of population enhancement by stocking, as well as its relevance for fishery management decision making.

evolutionary biology

Chromosomal fusion and life history-associated genomic variation contribute to within-river local adaptation of Atlantic salmon

Chromosomal inversions have been implicated in facilitating adaptation in the face of high levels of gene flow, but whether chromosomal fusions also have similar potential remains poorly understood. Atlantic salmon are usually characterized by population structure at multiple spatial scales; however, this is not the case for tributaries of the Miramichi River in North America. To resolve genetic relationships between populations in this system and the potential for known chromosomal fusions to contribute to adaptation we genotyped 728 juvenile salmon using a 50K SNP array. Consistent with previous work, we report extremely weak overall population structuring (Global FST = 0.004) and failed to support hierarchical structure between the rivers two main branches. We provide the first genomic characterization of a previously described polymorphic fusion between chromosomes 8 and 29. Fusion genomic characteristics included high LD, reduced heterozygosity in the fused homokaryotes, and strong divergence between the fused and the unfused rearrangement. Population structure based on fusion karyotype was five times stronger than neutral variation (FST = 0.019) and the frequency of the fusion was associated with summer precipitation supporting a hypothesis that this rearrangement may contribute local adaptation despite weak neutral differentiation. Additionally, both outlier variation among populations and a polygenic framework for characterizing adaptive variation in relation to climate identified a 250 Kb region of chromosome 9, including the gene six6 that has previously been linked to age-at-maturity and run-timing for this species. Overall our results indicate that adaptive processes, independent of major river branching, are more important than neutral processes for structuring these populations.

genomics

Intestinal microbiota of whitefish (Coregonus sp.) species pairs and their hybrids in natural and controlled environment.

It is becoming increasingly clear that wild animals have never existed without symbiotic interactions with microbiota. Therefore, investigating relationships between microbiota and their host is essential towards a full understanding of how animal evolve and adapt to their environment. The Lake Whitefish (Coregonus clupeaformis) is a well-documented model for the study of ecological speciation, where the dwarf species (limnetic niche specialist) evolved independently and repeatedly from the normal species (benthic niche specialist). In this study, we compared the transient intestinal microbiota among five wild sympatric species pairs of whitefish as well as captive representatives of dwarf and normal species and their reciprocal hybrids reared in identical controlled conditions. We sequenced the 16s rRNA gene V3-V4 regions of the transient intestinal microbiota present in a total of 185 whitefish to (i) test for parallelism in the transient intestinal microbiota among sympatric pairs of whitefish, (ii) test for transient intestinal microbiota differences among dwarf, normal and both hybrids reared under identical conditions and (iii) compare intestinal microbiota between wild and captive whitefish. A significant effect of host species on microbiota taxonomic composition was observed in the wild when all lakes where analyzed together, and species effect was observed in three of the five species pairs. In captive whitefish, an influence of host (normal, dwarf and hybrids) was also detected on microbiota taxonomic composition and tens of genera specific to dwarf, normal or hybrids were highlighted. Hybrid microbiota was not intermediate; instead its composition fell outside of that observed in the parental forms and this was observed in both reciprocal hybrid crosses. Interestingly, six genera formed a bacterial core which was present in captive and wild whitefish, suggesting a horizontal microbiota transmission. Although diet appeared to be a major driving force for microbiota evolution, our results suggested a more complex interaction among the host, the microbiota and the environment leading to three distinct evolutionary paths of the intestinal microbiota.

evolutionary biology

Convergent transcriptomic landscapes under polygenic selection accompany inter-continental parallel evolution within a Nearctic Coregonus (Salmonidae) sister-species complex.

In contrast to the plethora of studies focusing on the genomic basis of adaptive phenotypic divergence, the role of gene expression during speciation has been much less investigated and consequently, less understood. Yet, the convergence of differential gene expression patterns between closely related species-pairs might reflect the role of natural selection during the process of ecological speciation. Here, we test for intercontinental convergence in differential transcriptional signatures between limnetic and benthic sympatric species-pairs of Lake Whitefish (Coregonus clupeaformis) and its sister-lineage, the European Whitefish (C. lavaretus), using six replicated sympatric species-pairs (two in North America, two in Norway and two in Switzerland). We characterized both sequence variation in transcribed regions and differential gene expression between sympatric limnetic and benthic species across regions and continents. Our first finding was that differentially expressed genes (DEG) between limnetic and benthic whitefish tend to be enriched in shared polymorphism among sister-lineages. We then used both genotypes and co-variation in expression in order to infer polygenic selection at the gene level. We identified parallel outliers and DEG involving genes primarily over-expressed in limnetic species relative to the benthic species. Our analysis finally revealed the existence of shared genomic bases underlying parallel differential expression across replicated species pairs from both continents, such as a cis-eQTL affecting the pyruvate kinase expression level involved in glycolysis. Our results are consistent with a longstanding role of natural selection in maintaining transcontinental diversity at phenotypic traits involved in ecological speciation between limnetic and benthic whitefishes.

evolutionary biology

Sex-specific and conserved gene co-expression networks underlie phenotypes within the paleopolyploid Salvelinus genus (Family Salmonidae)

Networks of co-expressed genes produce complex phenotypes associated with functional novelty. Sex differences in gene expression levels or in the structure of gene co-expression networks can cause sexual dimorphism and may resolve sexually antagonistic selection. Here we used RNA-sequencing in the paleopolyploid salmonid Brook Charr Salvelinus fontinalis to characterize sex-specific co-expression networks in the liver of 35 female and 51 male offspring. In both networks, modules were characterized for functional enrichment, hub gene identification, and associations with 15 growth, reproduction, and stress-related phenotypes. Modules were then evaluated for preservation in the opposite sex, and in the congener Arctic Charr Salvelinus alpinus. Overall, more transcripts were assigned to a module in the female network than in the male network, which coincided with higher inter-individual gene expression and phenotype variation in the females. Most modules were preserved between sexes and species, including those involved in conserved cellular processes (e.g. translation, immune pathways). However, two sex-specific male modules were identified, and these may contribute to sexual dimorphism. To compare with the network analysis, differentially expressed transcripts were identified between the sexes, finding a total of 16% of expressed transcripts as sex-biased. For both sexes, there was no overrepresentation of sex-biased genes or sex-specific modules on the putative sex chromosome. Sex-biased transcripts were also not overrepresented in sex-specific modules, and in fact highly male-biased transcripts were enriched in preserved modules. Comparative network analysis and differential expression analyses identified different aspects of sex differences in gene expression, and both provided new insights on the genes underlying sexual dimorphism in the salmonid Brook Charr.

genomics

Karyotype-environment associations support a role for a chromosomal inversion in local adaptation among North American populations of the seaweed fly Coelopa frigida

Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialisation. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2,000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.

evolutionary biology

Parallel epigenetic modifications induced by hatchery rearing in a Pacific Salmon

Highlights- First study to highlight parallel epigenetic modifications induced by hatchery rearing as a potential explanatory mechanism for rapid change in fitness\n\nSummaryA puzzling question in conservation biology is how to maintain overall fitness of individuals bred in captive environment upon release into the wild, especially for rehabilitating declining or threatened species [1,2]. For salmonid species, a heritable change in fitness related traits and gene expression has been reported to occur in a single generation of captivity in hatchery environment [3-5]. Such rapid changes are congruent with models of inadvertent domestication selection which may lead to maladaptation in the natural environment [4]. Arguably, the underlying mechanism by which captivity may induce fitness difference between wild and captive congeners is still poorly understood. Short-term selection on complex phenotypic traits is expected to induce subtle changes in allele frequency over multiple loci [7-9]. Yet, most studies investigating the molecular basis for rapid change in fitness related traits occurring in hatchery have concentrated their effort on finding evidence for selection at the genome level by identifying loci with large effect.\n\nNumerous wild stocks of Pacific anadromous salmon and trout (genus Oncorhynchus and Salmo) have experienced fluctuating abundance over the past century, with a series of sharp declines [6-8]. With the objectives of preserving ecosystem integrity, enhancing declining populations and sustaining fisheries, conservation hatcheries have been flourishing. This is particularly true along the North American Pacific coast where billions of salmonids, all species included, are released each year. Despite substantial improvement of production management, the beneficial ecological role of hatcheries in enhancing and restoring wild stocks is still debated, mainly because of the reduced fitness and maladaptation of hatchery-fish when released in the wild [3,5,9]. Although previous studies showed that domestication selection was involved in such fitness impairment, they also observed that different environmental conditions (e.g. reduced fish density) significantly modulated the physiological acclimation to hatchery environment [4].\n\nEnvironmental stimuli are especially relevant during early embryonic development, which also correspond to a sensitive methylation reprogramming window in vertebrates [10,11]. It is therefore plausible that differences in rearing environment during early development may result in epigenetic modifications that could in turn impact on fitness. However, the only epigenetic study to date pertaining to captive rearing in salmonids and performed using methylation-sensitive amplified fragments (MSAP) failed to identify significant changes in methylation profile associated with hatchery rearing [12]\n\nHere, we used a higher resolution approach to compare the genome-wide pattern of methylation in hatchery-reared juvenile (smolt) Coho Salmon with that of their wild counterparts in two geographically distant rivers in British Columbia, Canada. Using a reduced representation bisulfite sequencing (RRBS) approach covering an average per individual of about 70 million cytosines in CpG context, we identified 100 methylated regions (DMRs) that differed in parallel between hatchery and natural origin salmon in both rivers. The total variance of epigenetic variation among individuals explained by river or origin and rearing environment in a RDA model was 16% (adj.R2=0.16), and both variables equally explained about 8% of the variance after controlling for each other. The gene ontology analysis revealed that regions with different methylation levels between hatchery and natural origin salmon showed enrichment for ion homeostasis, synaptic and neuromuscular regulation, immune and stress response, and control of locomotion functions. We further identified 15,044 SNPs that allowed detection of significant differences between either rivers or sexes. However, no effect of rearing environment was observed, confirming that hatchery and natural origin fish of a given river belong to the same panmictic population, as expected based on the hatchery programs applied in these rivers (see Supplementary experimental procedures). Moreover, neither a standard genome-scan approach nor a polygenic statistical framework allowed detection of selective effects within a single generation between hatchery and natural origin salmon. Therefore, this is the first study to demonstrate that parallel epigenetic modifications induced by hatchery rearing during early development may represent a potential explanatory mechanism for rapid change in fitness-related traits previously reported in salmonids.

genomics

Reconstructing The Demographic History Of Atlantic Salmon (Salmo salar) Across Its Distribution Range Using Approximate Bayesian Computations

Understanding the dual roles of demographic and selective processes in the buildup of population divergence is one of the most challenging tasks in evolutionary biology. In the Northern hemisphere in particular, species genetic makeup has been largely influenced by severe climatic oscillations of the Quaternary Period. Here, we investigated the demographic history of Atlantic Salmon across the entire species range using 2035 anadromous individuals from 77 sampling sites from North America and Eurasia genotyped at 4,656 SNPs. By combining results from admixture graphs, geogenetic maps and an approximate Bayesian computation framework, we validate previous hypotheses pertaining to secondary contact between European and Northern American populations, but also demonstrate that European populations from different glacial refugia have been exchanging alleles in contemporary times. We further identify the major sources of admixture from the southern range of North America to more northern populations along with a strong signal of secondary gene flow between genetic regional groups. We hypothesize that these patterns reflects the spatial redistribution of ancestral variation across the entire American range. Results also point to a role for linked selection in the form of background selection and or positive hitchhiking. Altogether, differential introgression and linked selective effects likely played an underappreciated role in shaping the genomic landscape of species in the Northern hemisphere Therefore we conclude that such heterogeneity among loci should be systematically integrated into demographic inferences of the divergence process, even between incompletely reproductively isolated populations.

evolutionary biology

Migration Harshness Drives Habitat Choice And Local Adaptation In Anadromous Arctic Char: Evidence From Integrating Population Genomics And Acoustic Telemetry

Migration is a ubiquitous life history trait with profound evolutionary and ecological consequences. Recent developments in telemetry and genomics, when combined, can bring significant insights on the migratory ecology of non-model organisms in the wild. Here, we used this integrative approach to document dispersal, gene flow and potential for local adaptation in anadromous Arctic Char from six rivers in the Canadian Arctic. Acoustic telemetry data from 124 tracked individuals indicated asymmetric dispersal, with a large proportion of fish (72%) tagged in three different rivers migrating up the same short river in the fall. Population genomics data from 6,136 SNP markers revealed weak, albeit significant, population differentiation (average pairwise FST = 0.011) and asymmetric dispersal was also revealed by population assignments. Approximate Bayesian Computation simulations suggested the presence of asymmetric gene flow, although in the opposite direction to that observed from the telemetry data, suggesting that dispersal does not necessarily lead to gene flow. These observations suggested that Arctic Char home to their natal river to spawn, but may overwinter in rivers with the shortest migratory route to minimize the costs of migration in non-breeding years. Genome scans and genetic-environment associations identified 90 outlier markers putatively under selection, 23 of which were in or near a gene. Of these, at least four were involved in muscle and cardiac function, consistent with the hypothesis that migratory harshness could drive local adaptation. Our study illustrates the power of integrating genomics and telemetry to study migrations in non-model organisms in logistically challenging environments such as the Arctic.

evolutionary biology

Sex chromosome evolution, heterochiasmy and physiological QTL in the salmonid Brook Charr Salvelinus fontinalis

Whole genome duplication can have large impacts on genome evolution. However, much remains unknown about these impacts, such as the mechanisms of coping with a duplicated sex determination system, which may result in increased sex determination mechanism diversity. Sexual conflict (i.e. alleles having different optimums in each sex) can result in sequestration of genes into non-recombining sex chromosomes. Development of sex chromosomes may involve heterochiasmy (i.e. sex-specific recombination rate), which is also poorly understood. Family Salmonidae is a model system for these phenomena, having undergone autotetraploidization and subsequent rediploidization in most of the genome at the base of the lineage. The salmonid master sex determining gene is known, and many species have non-homologous sex chromosomes, putatively due to transposition of this gene. In this study, we identify the sex chromosome of Brook Charr Salvelinus fontinalis and compare sex chromosome identities across the lineage (eight species, four genera). Although non-homology is frequent, homologous sex chromosomes and other consistencies are present in distantly related species, indicating probable convergence on specific sex and neo-sex chromosomes. We also characterize strong heterochiasmy with 2.7-fold more crossovers in maternal than paternal haplotypes with paternal crossovers biased to chromosome ends. Y chromosome crossovers are restricted to a single end of the chromosome, and this chromosome contains a large interspecific inversion, although its status between males and females remains unknown. Finally, we identify QTL for 21 unique growth, reproductive and stress-related phenotypes to improve knowledge of the genetic architecture of these traits important to aquaculture and evolution.

genomics

Sex matters in Massive Parallel Sequencing: Evidence for biases in genetic parameter estimation and investigation of sex determination systems

Using massively parallel sequencing data from two species with different life history traits -- American lobster (Homarus americanus) and Arctic Char (Salvelinus alpinus) -- we highlighted how an unbalanced sex ratio in the samples combined with a few sex-linked markers may lead to false interpretations of population structure and thus to potentially erroneous management recommendations. Multivariate analyses revealed two genetic clusters that separated males and females instead of showing the expected pattern of genetic differentiation among ecologically divergent (inshore vs. offshore in lobster) or geographically distant (east vs. west in Arctic Char) sampling locations. We created several subsamples artificially varying the sex ratio in the inshore/offshore and east/west groups, and then demonstrated that significant genetic differentiation could be observed despite panmixia for lobster, and that Fst values were overestimated for Arctic Char. This pattern was due to 12 and 94 sex-linked markers driving differentiation for lobster and Arctic Char, respectively. Removing sex-linked markers led to nonsignificant genetic structure (lobster) and a more accurate estimation of Fst (Arctic Char). We further characterized the putative functions of sex-linked markers. Given that only 9.6% of all marine/diadromous population genomic studies to date reported sex information, we urge researchers to collect and consider individual sex information. In summary, we argue that sex information is useful to (i) control sex ratio in sampling, (ii) overcome \"sex-ratio bias\" that can lead to spurious genetic differentiation signals and (iii) fill knowledge gaps regarding sex determining systems.

genomics

Functional Analysis of All Salmonid Genomes (FAASG): an international initiative supporting future salmonid research, conservation and aquaculture

We describe an emerging initiative - the Functional Analysis of All Salmonid Genomes (FAASG), which will leverage the extensive trait diversity that has evolved since a whole genome duplication event in the salmonid ancestor, to develop an integrative understanding of the functional genomic basis of phenotypic variation. The outcomes of FAASG will have diverse applications, ranging from improved understanding of genome evolution, through to improving the efficiency and sustainability of aquaculture production, supporting the future of fundamental and applied research in an iconic fish lineage of major societal importance.

genomics